Value-Related Neuronal Responses in the Human Amygdala during Observational Learning

• Published in: The Journal of neuroscience Vol. 40; no. 24; pp. 4761 - 4772
• Main Authors: Aquino, Tomas G, Minxha, Juri, Dunne, Simon, Ross, Ian B, Mamelak, Adam N, Rutishauser, Ueli, O'Doherty, John P
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 10.06.2020
• Subjects: Amygdala; Amygdala - physiology; Coding; Cognition; Cognition - physiology; Computational neuroscience; Decoding; Female; Humans; Learning; Learning - physiology; Male; Models, Neurological; Neural coding; Neurons; Neurons - physiology; Neurosurgery; Observational learning; Reagents; Reinforcement; Social discrimination learning; Social interactions; Social Perception; Stimuli; human electrophysiology; observational learning; social cognition; intracranial recordings; decision making; reinforcement learning
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.2897-19.2020

The amygdala plays an important role in many aspects of social cognition and reward learning. Here, we aimed to determine whether human amygdala neurons are involved in the computations necessary to implement learning through observation. We performed single-neuron recordings from the amygdalae of human neurosurgical patients (male and female) while they learned about the value of stimuli through observing the outcomes experienced by another agent interacting with those stimuli. We used a detailed computational modeling approach to describe patients' behavior in the task. We found a significant proportion of amygdala neurons whose activity correlated with both expected rewards for oneself and others, and in tracking outcome values received by oneself or other agents. Additionally, a population decoding analysis suggests the presence of information for both observed and experiential outcomes in the amygdala. Encoding and decoding analyses suggested observational value coding in amygdala neurons occurred in a different subset of neurons than experiential value coding. Collectively, these findings support a key role for the human amygdala in the computations underlying the capacity for learning through observation. Single-neuron studies of the human brain provide a unique window into the computational mechanisms of cognition. In this study, epilepsy patients implanted intracranially with hybrid depth electrodes performed an observational learning (OL) task. We measured single-neuron activity in the amygdala and found a representation for observational rewards as well as observational expected reward values. Additionally, distinct subsets of amygdala neurons represented self-experienced and observational values. This study provides a rare glimpse into the role of human amygdala neurons in social cognition.